impact of different tree species on soil phosphorus ... · keywords: soil phosphorus...

$: Impact of different tree species on soil phosphorus ... · Keywords: Soil phosphorus bioavailability, organic phosphorus mineralisation, soil phosphorus fractionation, Pinus radiate,$
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Journal of Soil Science and Plant Nutrition, 2016, 16 (2), 477-489

RESEARCH ARTICLE

Impact of different tree species on soil phosphorus immediately following grassland afforestation

I. Chirino-Valle1, M. R. Davis2, L.M. Condron1*

1Agriculture and Life Sciences, PO Box 85084, Lincoln University, Lincoln 7647, Christchurch, New Zealand. 2Scion, PO Box 29237, Fendalton, Christchurch, New Zealand.*Corresponding Author: [email protected]

Abstract

Previous studies have revealed that significant changes in soil phosphorus (P) occurred as a consequence of grassland afforestation, although when these changes occurred and the influence of different tree species re-mains largely unknown. This study involved assessing changes in soil phosphorus (P) over a 10 year period fol-lowing the afforestation of grazed pasture with 3 contrasting tree species (Pinus radiata, Cupressus macrocarpa, Eucalyptus nitens) in a replicated field trial at Orton Bradley Park, New Zealand. A combination of techniques (sequential fractionation, alkaline phosphatase hydrolysable P, solution 31P nuclear magnetic resonance spectros-copy) was used to quantify changes in the nature and bioavailability of soil P. Results revealed that the establish-ment and growth of trees caused a significant decrease in soil organic P within 10 years, indicating net organic P mineralisation. Surprisingly this trend was similar under all three tree species, which suggested similar soil P acquisition despite differences in the type of mycorrhizae associated with each species: P. radiata is ectomycor-rhizal, C. macrocarpa is arbuscular mycorrhizal, and E. nitens can beectomycorrhizal or arbuscular mycorrhizal. The observed changes in soil P dynamics were attributed a combination of tree growth and P uptake irrespective of species and changes in P inputs and organic P turnover associated with the cessation of grazing following tree planting. Changes in the nature of organic P determined 10 years after establishment indicated that organic matter inputs associated with tree growth were having an increasing influence on soil P dynamics with time.

Keywords: Soil phosphorus bioavailability, organic phosphorus mineralisation, soil phosphorus fractionation, Pinus radiate, Cupressus macrocarpa, Eucalyptus nitens


478 Chirino et al.

1. Introduction

Native and managed plantation forests account for one third of the land area in New Zealand and play a vital role in the country’s ecological, environmen-tal and socio-economic prosperity and sustainability. These forest ecosystems provide an ideal template to investigate and quantify the key properties and pro-cesses that drive soil nutrient dynamics and bioavail-ability, including phosphorus (P).Between 1985 and 2000 almost 1 million hectares of improved grassland (i.e. grazed fertilized pasture established following clearance of native forest) was converted to short-rotation plantation forestry which was predominantly radiata pine (Pinus ra-diata). This dramatic land-use change was mainly driven by declines in the economic viability of pas-toral farming in many hill and high country areas of New Zealand (Davis, 1998; Glass, 1997). In the absence of replicated long-term field experiments under contrasting land-uses, investigation of the impacts of grassland afforestation on soil proper-ties and processes relied on paired-site comparisons at a single point in time after forest establishment (Chen et al., 2000; Condron et al., 1996b; Davis and Lang, 1991). This approach involved using transects to sample soil under adjacent grassland and recently established forest, which was effectively a form of pseudo-replication. Nonetheless, a large number of such paired-site comparison studies were carried out in New Zealand, and consistently revealed that sig-nificant changes occurred in the amounts and forms of soil P as a consequence of afforestation, result-ing in enhanced mineralization of organic P and concomitant significant increases in plant-available inorganic P (Chen et al., 2008). The pair-site comparison studies cited above could not show how soil P changed with time following land-use change, and assessment of changes in soil P

with time following forest establishment would pro-vide more information on the mechanisms responsible for enhanced mineralization of soil organic P. Fur-thermore, there is very little known about the effects of different plantation forest tree species other than radiata pine, which in turn may also provide some insight into the mechanisms responsible for the dra-matic changes in soil P associated with afforestation of grassland (Chen et al., 2008). The main objective of this study was to determine changes in the chemi-cal nature and availability of topsoil P over a period of 10 years following afforestation of long-established grazed hill country pasture in a replicated field experi-ment which included three contrasting plantation for-est tree species.

2. Materials and Methods

2.1. Study site and soil sampling

Orton Bradley Park is located near Charteris Bay on Banks Peninsula, Canterbury, New Zealand (43o 39´ S, 172o 42´ E). The soil is a Takahe silt loam (Mottled FragicPallic soil, NZ classification; TypicFragiustept, USDA classification) formed in greywacke loess. The altitude is 100-150 m, mean annual rainfall is ap-proximately 1000 mm and mean annual temperature is 12.1oC. A replicated afforestation trial was estab-lished in 1999 at Orton Bradley Park in an area that had been developed under grazed pasture with limited fertilizer inputs on a north-east facing slope at 70-150 m elevation. The trial comprised 4 replicates of three contrasting commercial plantation forest trees (radiata pine, Cupressus macrocarpa [macrocarpa], Eucalyp-tus nitens [eucalyptus]) arranged in a randomized block design of twelve plots each measuring 30 m x 30 m. The plots were developed under grazed pasture


479Impact of different tree species on soil phosphorus

[macrocarpa], Eucalyptus nitens [eucalyptus]) ar-ranged in a randomized block design of twelve plots each measuring 30 m x 30 m. The plots were devel-oped under grazed pasture (Lolium perenne and Tri-foilum repens) with low rates of superphosphate fer-tilizer inputs (˂100 kg ha-1). The plots were fenced off at trial establishment and trees were planted at 1250 stems/ha (Huang et al., 2011).The plots were not grazed or fertilized since tree planting and trees were pruned and thinned in accordance with com-mercial silvicultural practice. Data presented in Table 1 shows values of pH, Total C and Total N in the topsoil (0-5 cm). After ten years of afforestation,

the plots under P. radiata showed a thick litter layer with 2 to 11 cm in thickness. The amount of litter found under E. nitens and C. macrocarpa was negli-gible (Huang et al., 2011). A detailed soil sampling protocol was developed for the trial at its inception in 1999. Samples of mineral topsoil (0-5 cm) were taken using a 6 cm diameter corer from five sites ran-domly located near the middle of each replicate plot in spring (September-October) in 1999 and 2009. For each sampling event, soil samples were collected from each of the 4 replicate plots of each species (12 plots), and were air-dried, sieved <2 mm and stored prior to analysis.

Table 1. Soil properties in the 0-5 cm layer at the time of planting, and 10 years after afforestation. Means ( ± standard deviation) are based on four replicates

2.2. Soil analysesVarious forms of extractable soil inorganic P (Pi) and organic P (Po) were determined using the sequential fractionation scheme outlined by Chen et al. (2000), which in turn was a modification of the method devel-oped by Hedley et al. (1982). This scheme involved sequential extraction of 1g soil with 1M NaCl, 0.5M NaHCO3 (pH 8.5), 0.1M NaOH (NaOH-I),1M HCl and 0.1M NaOH (NaOH-II). Labile P was represented by the sum of the most readily extracted forms of P (NaCl Pi and NaHCO3 Pi). Total extractable Pi was the

sum of labile P, NaOH-I Pi, HCl-Pi and NaOH-II Pi, while total extractable Po was the sum of NaHCO3 Po, NaOH-I Po and NaOH-II Po. Following the method proposed by O'Halloran and Cade-Menun (2008) al-kaline phosphatase (from Escherichia coli, SIGMA, USA) enzyme hydrolysable P was determined in NaHCO3 extracts of air dried <2 mm sieved 0-5cm soils collected in 1999 and 2009 under radiata pine. Detailed analyses of organic P forms using 31P nuclear magnetic resonance spectroscopy (NMR) analysis of NaOH-EDTA extractable organic P from was carried


480 Chirino et al.

out on the same soil samples collected under Pinus radiata, using a standard protocol described by Turner et al. (2003), although extracts from each of the 4 replicates from each year were combined for NMR analysis.

2.3. Statistical analysis

One and two way analysis of variance (ANOVA) were carried out on the data to test for the effects of sampling year (1999 and 2009) and tree species on soil P fractions. One way ANOVA was also carried out to test the temporal effects on the enzyme labile P. Where F ratios were significant treatment means were compared by least significant differences (lsd).

3. Results

Data presented in Table 2 shows the ANOVA F val-ues and their levels of significance for all of the soil P fractions for the different tree species and years of sampling, together with the corresponding interac-tion. There were no significant differences observed between the three tree species for any of the soil P fractions, although significant differences (p<0.05) occurred between sampling years for NaHCO3Po, NaOH-IPo, NaOH-II Po and total extractable Po. Accordingly, data for labile P, NaOH-IPo, HClPi, NaOH- II Pi, NaOH-II Po and total extractable Po av-eraged across all tree species for samples taken in 1999 and 2009 for 0-5 cm soil are shown in Figure 1.

Table 2. F values with levels of significance from analyses of variance for all the soil P fractions for species and year and the interaction between species and year (Sp x Y) for 0-5cm soil. Numbers in bold show significant differences (p ˂0.05).



Figure 1. Mean concentrations (mgP /kg) in different P fractions determined for 0-5 cm soil sampled in 1999 and 2009 averaged over the three tree species (radiata pine, macrocarpa, eucalyptus). The error bars represent stan-dard errors of means. Different letters indicate that means differ significantly between sampling years (p ˂ 0.05).

Labile P,NaHCO3 Po, NaOH I-Pi and total extractable Pi did not show significant changes among years, and while concentrations of NaOH-I Po and HClPi de-creased significantly between 1999 and 2009, NaOH-II Pi and NaOH-II Po increased significantly between 1999 and 2009. Total extractable Po decreased signifi-cantly between 1999 and 2009. Alkaline phosphatase hydrolysable P decreased significantly between 1999 and 2009 from 70 to 50 mgP/kg (Figure 2).

Table 3 shows the concentration of P compounds de-termined by 31P NMR in extracts of 0-5 cm soils under radiata pine sampled in 1999 and 2009. The sum of all phosphate monoesters accounted for 92-96% of the Po compounds detected, and decreased with time from 408 mg P/kg in 1999 to 343 mg P/kg in 2009. This was mainly due to decreases in the “other monoester” frac-tion, while the only other change noted was a fourfold increase in phosphonate-P between 1999 and 2009.


482 Chirino et al.

Figure 2. Mean concentrations of alkaline phosphatase hydrolysable P (mgP /kg) determined for NaHCO3 ex-tracts from 0-5cm soil sampled under radiata pine in 1999, 2004 and 2009. The error bars represent standard errors of means. Different letters indicate that means differ significantly between sampling years (p ˂ 0.05).

Table 3. Concentrations (mgP /kg) of different organic P compounds determined by 31P NMR analysis of NaOH-EDTA extracts of 0-5 cm soils sampled under radiata pine in 1999 and 2009. Values in parentheses are the propor-tion (%) of the total P extracted by NaOH-EDTA.

4. Discussion

It was hypothesised that the quantities and nature of soil P would change during the 10 years following af-forestation and that any changes in soil P would be af-fected by tree species. However, the three tree species had a very similar overall impact on the amounts and forms of P determined over the first 10 years follow-ing establishment. This was particularly surprising

given the different growth rates of the three tree spe-cies (Table 5), which were clearly demonstrated in their different impact on the grassland understorey. After 10 years (2009), complete canopy closure was evident in the P. radiata plots and the grassland un-derstory had been effectively buried under a combi-nation of needle litter and course wood debris from thinning and pruning (Figure 3) (Figure 4). On the other hand, there was no grassland understory evident



under E. nitens, which was probably attributable to competition for soil moisture by the trees. Over the same period, the grassland understory persisted un-der C. macrocarpa, which probably reflected slower growth rates compared with P. radiata and E. nitens. The fact that NaOH-I Po and total extractable Po de-creased significantly between 1999 and 2009 indi-cated that forest establishment had resulted in net

Figure 3. Status of the understory under a) Pinus radiata, b) Cupressus macrocarpa and c) Eucalyptus nitens in 1999.

Figure 4. Status of the understory under a) Pinus radiata, b)Cupressus macrocarpa and c) Eucalyptus nitens in 2009.

mineralization of soil organic P. This is consistent with previous paired site comparison studies which showed that significant mineralization of soil organ-ic P occurred 10-20 years after the change in land-use (Chen et al., 2000; Condron et al., 1996a; Davis and Lang, 1991; Hawke and O’Connor, 1993)


484 Chirino et al.

It is also possible that the significant decrease ob-served between 1999 and 2009 could be associated with bulk density changes promoted by the growth of tree roots, but unfortunately there is not data available to be compared between those years. An-other explanation is that the organic forms of P were relocated in a non-extractable pool that was not ob-served through the fractionation method used here, however, the percentage of the organic fractions with respect to the total extractable Po showed a similar trend than that for concentrations (Table 4). Differ-ences associated with soil sampling between years that altered the amount of total P would also have ex-plained this behaviour. Phosphorus uptake by newly established trees may at least partly explain the en-hanced mineralization of soil organic P, although it was surprising that this was similar under all three tree species despite differences in mycorrhizal asso-ciations, root physiology and growth rates. In partic-ular, it was expected that differences in mycorrhizae between P. radiata (ectomycorrhizae [EM]), C. mac-rocarpa (vesicular-arbuscular mycorrhizae [VAM]) and E. nitens (EM/VAM) would result in different impacts on soil P. Previous studies have showed that short-term mineralization of rhizosphere soil organic P was significantly greater for radiata pine compared with perennial ryegrass (Lolium perenne) which has VAM (Chen et al., 2002). The fact that soil organic P decreases were similar under all three tree species suggests that EM and VAM were equally effective at mobilising organic P by mineralisation, which is contrary to current understanding of the role of dif-ferent mycorrhizal types in P acquisition (Chen et al., 2002; Lambers et al., 2008; Read and Perez-Moreno, 2003; Smith et al., 2008; Smith and Read, 2008) al-though it is consistent with recent findings from trop-ical montane tree species (Steidinger et al., 2015). Tree biomass measurements taken in 2009 showed that standing stem volumes (m3/ha) were greater

for P. radiata (211) and E. nitens (165) compared with C. macrocarpa (109) (Table 5). There was no corresponding data available for P content of the tree biomass, but the fact that changes in soil P were simi-lar for all three tree species may indicate comparable quantities of biomass P uptake. It is also possible that changes in P cycling associated with the cessation of grazing following tree planting could have contributed to the immediate significant decline in soil organic P. This in turn may be attributed to changes in the quantities of P being returned to soil and its consequent impacts on the balance between the respective rates of organic P inputs and turnover, especially since the NaHCO3 and NaOH-I P fractions are generally considered to represent the more labile pools of soil organic P (Condron et al., 2005). This suggests that the quantity and turnover of organic P in soil may have been reduced following the cessation of grazing. Grazing animals play a very important role in the process of P cycling in pasture ecosystems since 95% of the P taken up by plants is returned to the soil in the form of feces and root residues (Haynes and Williams, 1993; Kemp et al., 2000), which in turn enhances biological cycling of P (Nash et al., 2014).Simpson et al. (2012) investigated the relative solu-bility of soil P under contrasting mowing regimes (no mowing, clippings removed, clippings left) which had been maintained in a field trial for 15 years. In approximate terms, the regime where clippings were left was equivalent to grazing while no mowing would be equivalent the situation at Orton Bradley Park following the cessation of grazing when trees were planted. They showed that biological and bio-chemical processes associated with enhanced min-eralization of organic P were significantly greater in soils where were clipping left compared to no mow-ing, which reflected increased organic matter inputs under the clippings return regime.



Table 4. Mean percentage (%) of labile P, NaHCO3 Po, NaOH-I Pi, NaOH-I Po, HCl Pi, NaOH-II Pi, and NaOH-II Po and mean concentration (mg P/kg) of total extractable Pi and Po fractions under P. radiata, C. macrocarpa and E. nitens in 1999 and 2009.

*Labile P is the sum of inorganic and organic P in NaCl; **ƩPi is the sum of inorganic P in NaCl, NaHCO3, NaOH-I, HCl, and

NaOH-II; ***ƩPo is the sum of organic P in NaCl, NaHCO3, NaOH-I and NaOH-II, **** ƩP is the sum of ƩPi + ƩPo.

Table 5. Comparative growth of the three tree species determined 10 years after planting (2009) (standard errors are shown in parenthesis).


486 Chirino et al.

In addition, studies of long-term changes in soil P under grazed pasture in New Zealand and elsewhere have clearly and consistently demonstrated that con-centrations of soil organic P increased significantly with time. This was attributed to elevated rates of organic matter and P inputs and turnover compared with soils under unimproved and native vegetation (Tiessen and Condron, 2005; Condron et al., 2005; McDowell and Condron, 2012).Previous paired-site studies clearly showed that both the size and activity of the soil microbial biomass, together with phosphatase enzyme activities, were consistently and significantly lower under forest compared with adjacent grassland (Chen et al., 2003; Chen et al., 2008). He et al. (1997) concluded that fluctuations in the size and turnover of soil microbial biomass were very important to control the turnover of C, N and P, which in turn regulate plant availability of P. Chen et al. (2003) reported that concentrations of microbial biomass P were higher in grasslands compared to adjacent forest and concluded that it was mainly affected by returns of grass root litter in the first and by litterfall accumulation in the second. Increases in non-labile NaOH-II Po that occurred be-tween 1999 and 2009 may indicate a shift towards more recalcitrant organic matter in soil reflecting increased inputs of organic matter and P from tree residues and roots. Huang et al. (2011) analysed soils taken from the Orton Bradley Park trial over the same period (1999-2009) to quantify changes in soil C mass in light and heavy fractions. Although they found that C mass did not show significant differences in the soil heavy fraction, C mass in the light fraction displayed a similar pattern to that found in this study for NaOH-II Po (most recalcitrant) by increasing its concentra-tion between 1999 and 2009. They attributed the increased of C mass between year 1999 and 2009 to C inputs from tree residues. Condron and Newman (1998) used 13C-NMR spectroscopy to investigate the

chemical nature of the soil organic C under grassland and adjacent recently established coniferous forests (10-17 years). They found that under grassland the soil organic C was closely related to plant fragments and partially degraded residues derived from grass roots, while soil organic C was more recalcitrant un-der forest These changes in soil organic C are consis-tent with the increases in the recalcitrant NaOH-II Po fraction that was observed between 1999 and 2009. As the turnover of C in a system increases through plant addition, the biological processes of mineraliza-tion determine the availability of P (Bünemann and Condron, 2007; Richardson et al., 2004). Further-more, labile organic P could be mineralised by greater microbial activity to meet increasing plant demand in the early stages of tree establishment.Specific results determined for changes in enzyme hy-drolysable P and organic P under P. radiata over 10 years provided some important additional perspective on the nature of changes that occurred following tree planting. The fact that alkaline phosphatase hydro-lysable P decreased significantly between 1999 and 2009, indicates that while the solubility of organic P in NaHCO3 increased between 1999 and 2009, its susceptibility to enzyme mineralisation (i.e. its la-bility) actually decreased. The latter may indicate a shift towards more recalcitrant soil organic matter be-tween 1999 and 2009 as discussed above. However, differences in soil organic P solubility and enzyme lability also highlights limitations in assigning rela-tive lability/stability based on ease of extraction from soil (Condron and Newman, 2011). The NMR data showed that monoester forms of organic P decreased as a consequence of afforestation of grassland , which is consistent with studies which compared changes in soil organic P under radiata pine-and perennial rye-grass (Turner et al., 2005). However, the decreases in organic P determined in the present study were con-fined to “other monoesters”, while the other studies



noted significant depletion of scyllo and myo inositol hexakisphosphates. This may be at least partly related to the fact that the comparative studies cited above were carried out on soils from a 10 month glasshouse pot trial, as opposed to changes determined over 10 years under field conditions in the present study. The occurrence of phosphonates P in soil is linked to acid-ity (Condron et al., 2005), and the increase observed between 1999 and 2009 may be at least partly be at-tributed to a decline in soil pH on the trial from 4.9 in 1999 to 4.4-4.5 in 2009. This pH decline under trees may also account for the significant decrease in HCl Pi that occurred between 1999 and 2009 (Figure 1).

5. Conclusions

The findings of this study confirmed that signifi-cant net mineralisation of soil organic P occurred during the 10years following tree planting, but that this was similar under the three contrasting tree spe-cies despite differences in growth and mycorrhizal association. The latter suggested that EM and AM were equally effective at mineralizing soil organic P, and the observed changes in soil P could be at-tributed to tree growth and P uptake irrespective of species. However, reductions in P inputs and organic P turnover associated with the cessation of grazing may have also contributed to enhanced soil organic P mineralisation following forest establishment. In ad-dition, changes in the nature of organic P determined between 0-10 years after establishment indicated that organic matter inputs and turnover associated with tree growth were having an increasing influence on soil P dynamics with time.

Acknowledgements

Funding for establishment and maintenance of the field trial at Orton Bradley Park was provided by the C Alma Baker Trust, the Brian Mason Scientific and Technical Trust and Lincoln University. The contin-ued support provided by the Trustees of Orton Brad-ley Park is greatly appreciated. ICV was supported by a Lincoln University Doctoral scholarship.

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